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Biochem J. Sep 15, 2002; 366(Pt 3): 689–704.
PMCID: PMC1222826

Phagosome maturation: aging gracefully.


Foreign particles and apoptotic bodies are eliminated from the body by phagocytic leucocytes. The initial stage of the elimination process is the internalization of the particles into a plasma membrane-derived vacuole known as the phagosome. Such nascent phagosomes, however, lack the ability to kill pathogens or to degrade the ingested targets. These properties are acquired during the course of phagosomal maturation, a complex sequence of reactions that result in drastic remodelling of the phagosomal membrane and contents. The determinants and consequences of the fusion and fission reactions that underlie phagosomal maturation are the topic of this review.

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Selected References

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  • Tjelle TE, Lovdal T, Berg T. Phagosome dynamics and function. Bioessays. 2000 Mar;22(3):255–263. [PubMed]
  • Berón W, Alvarez-Dominguez C, Mayorga L, Stahl PD. Membrane trafficking along the phagocytic pathway. Trends Cell Biol. 1995 Mar;5(3):100–104. [PubMed]
  • Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. 1999;17:593–623. [PubMed]
  • Bangs P, Franc N, White K. Molecular mechanisms of cell death and phagocytosis in Drosophila. Cell Death Differ. 2000 Nov;7(11):1027–1034. [PubMed]
  • Franc NC, White K, Ezekowitz RA. Phagocytosis and development: back to the future. Curr Opin Immunol. 1999 Feb;11(1):47–52. [PubMed]
  • May RC. Phagocytosis in C. elegans: CED-1 reveals its secrets. Trends Cell Biol. 2001 Apr;11(4):150–150. [PubMed]
  • Platt N, da Silva RP, Gordon S. Class A scavenger receptors and the phagocytosis of apoptotic cells. Immunol Lett. 1999 Jan;65(1-2):15–19. [PubMed]
  • Cardelli J. Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide-based processes, biochemically distinct. Traffic. 2001 May;2(5):311–320. [PubMed]
  • Duclos S, Desjardins M. Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol. 2000 Oct;2(5):365–377. [PubMed]
  • Hackstadt T. Redirection of host vesicle trafficking pathways by intracellular parasites. Traffic. 2000 Feb;1(2):93–99. [PubMed]
  • Méresse S, Steele-Mortimer O, Moreno E, Desjardins M, Finlay B, Gorvel JP. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat Cell Biol. 1999 Nov;1(7):E183–E188. [PubMed]
  • Rabinovitch M. Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 1995 Mar;5(3):85–87. [PubMed]
  • Kwiatkowska K, Sobota A. Signaling pathways in phagocytosis. Bioessays. 1999 May;21(5):422–431. [PubMed]
  • Caron E, Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science. 1998 Nov 27;282(5394):1717–1721. [PubMed]
  • Indik ZK, Park JG, Hunter S, Schreiber AD. The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood. 1995 Dec 15;86(12):4389–4399. [PubMed]
  • Nagarajan S, Chesla S, Cobern L, Anderson P, Zhu C, Selvaraj P. Ligand binding and phagocytosis by CD16 (Fc gamma receptor III) isoforms. Phagocytic signaling by associated zeta and gamma subunits in Chinese hamster ovary cells. J Biol Chem. 1995 Oct 27;270(43):25762–25770. [PubMed]
  • Ofek I, Goldhar J, Keisari Y, Sharon N. Nonopsonic phagocytosis of microorganisms. Annu Rev Microbiol. 1995;49:239–276. [PubMed]
  • Schütt C. Fighting infection: the role of lipopolysaccharide binding proteins CD14 and LBP. Pathobiology. 1999;67(5-6):227–229. [PubMed]
  • Daëron M. Fc receptor biology. Annu Rev Immunol. 1997;15:203–234. [PubMed]
  • Gessner JE, Heiken H, Tamm A, Schmidt RE. The IgG Fc receptor family. Ann Hematol. 1998 Jun;76(6):231–248. [PubMed]
  • Petty HR, Todd RF., 3rd Receptor-receptor interactions of complement receptor type 3 in neutrophil membranes. J Leukoc Biol. 1993 Nov;54(5):492–494. [PubMed]
  • Yefenof E. Complement receptor 3 (CR3): a public transducer of innate immunity signals in macrophages. Adv Exp Med Biol. 2000;479:15–25. [PubMed]
  • Sansonetti PJ. Phagocytosis, a cell biology view. J Cell Sci. 2000 Oct;113(Pt 19):3355–3356. [PubMed]
  • Joiner KA, Ganz T, Albert J, Rotrosen D. The opsonizing ligand on Salmonella typhimurium influences incorporation of specific, but not azurophil, granule constituents into neutrophil phagosomes. J Cell Biol. 1989 Dec;109(6 Pt 1):2771–2782. [PMC free article] [PubMed]
  • Bouvier G, Benoliel AM, Foa C, Bongrand P. Relationship between phagosome acidification, phagosome-lysosome fusion, and mechanism of particle ingestion. J Leukoc Biol. 1994 Jun;55(6):729–734. [PubMed]
  • Pitt A, Mayorga LS, Stahl PD, Schwartz AL. Alterations in the protein composition of maturing phagosomes. J Clin Invest. 1992 Nov;90(5):1978–1983. [PMC free article] [PubMed]
  • Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood. 1998 Nov 1;92(9):3007–3017. [PubMed]
  • Tapper H. The secretion of preformed granules by macrophages and neutrophils. J Leukoc Biol. 1996 May;59(5):613–622. [PubMed]
  • Lemmon SK, Traub LM. Sorting in the endosomal system in yeast and animal cells. Curr Opin Cell Biol. 2000 Aug;12(4):457–466. [PubMed]
  • Barbieri MA, Roberts RL, Mukhopadhyay A, Stahl PD. Rab5 regulates the dynamics of early endosome fusion. Biocell. 1996 Dec;20(3):331–338. [PubMed]
  • Mukherjee S, Ghosh RN, Maxfield FR. Endocytosis. Physiol Rev. 1997 Jul;77(3):759–803. [PubMed]
  • McMahon HT. Endocytosis: an assembly protein for clathrin cages. Curr Biol. 1999 May 6;9(9):R332–R335. [PubMed]
  • Riezman H, Woodman PG, van Meer G, Marsh M. Molecular mechanisms of endocytosis. Cell. 1997 Dec 12;91(6):731–738. [PubMed]
  • Woodman PG. Biogenesis of the sorting endosome: the role of Rab5. Traffic. 2000 Sep;1(9):695–701. [PubMed]
  • Mohrmann K, van der Sluijs P. Regulation of membrane transport through the endocytic pathway by rabGTPases. Mol Membr Biol. 1999 Jan-Mar;16(1):81–87. [PubMed]
  • Somsel Rodman J, Wandinger-Ness A. Rab GTPases coordinate endocytosis. J Cell Sci. 2000 Jan;113(Pt 2):183–192. [PubMed]
  • Thilo L, Stroud E, Haylett T. Maturation of early endosomes and vesicular traffic to lysosomes in relation to membrane recycling. J Cell Sci. 1995 Apr;108(Pt 4):1791–1803. [PubMed]
  • Gruenberg J. The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol. 2001 Oct;2(10):721–730. [PubMed]
  • Gruenberg J, Maxfield FR. Membrane transport in the endocytic pathway. Curr Opin Cell Biol. 1995 Aug;7(4):552–563. [PubMed]
  • Gu F, Gruenberg J. Biogenesis of transport intermediates in the endocytic pathway. FEBS Lett. 1999 Jun 4;452(1-2):61–66. [PubMed]
  • Desjardins M, Huber LA, Parton RG, Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol. 1994 Mar;124(5):677–688. [PMC free article] [PubMed]
  • Desjardins M, Nzala NN, Corsini R, Rondeau C. Maturation of phagosomes is accompanied by changes in their fusion properties and size-selective acquisition of solute materials from endosomes. J Cell Sci. 1997 Sep;110(Pt 18):2303–2314. [PubMed]
  • Mayorga LS, Bertini F, Stahl PD. Fusion of newly formed phagosomes with endosomes in intact cells and in a cell-free system. J Biol Chem. 1991 Apr 5;266(10):6511–6517. [PubMed]
  • Jahraus A, Tjelle TE, Berg T, Habermann A, Storrie B, Ullrich O, Griffiths G. In vitro fusion of phagosomes with different endocytic organelles from J774 macrophages. J Biol Chem. 1998 Nov 13;273(46):30379–30390. [PubMed]
  • Mills IG, Jones AT, Clague MJ. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol. 1998 Jul 16;8(15):881–884. [PubMed]
  • Scianimanico S, Desrosiers M, Dermine JF, Méresse S, Descoteaux A, Desjardins M. Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes. Cell Microbiol. 1999 Jul;1(1):19–32. [PubMed]
  • Duclos S, Diez R, Garin J, Papadopoulou B, Descoteaux A, Stenmark H, Desjardins M. Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J Cell Sci. 2000 Oct;113(Pt 19):3531–3541. [PubMed]
  • Botelho RJ, Hackam DJ, Schreiber AD, Grinstein S. Role of COPI in phagosome maturation. J Biol Chem. 2000 May 26;275(21):15717–15727. [PubMed]
  • Muller WA, Steinman RM, Cohn ZA. The membrane proteins of the vacuolar system. II. Bidirectional flow between secondary lysosomes and plasma membrane. J Cell Biol. 1980 Jul;86(1):304–314. [PMC free article] [PubMed]
  • Pitt A, Mayorga LS, Schwartz AL, Stahl PD. Transport of phagosomal components to an endosomal compartment. J Biol Chem. 1992 Jan 5;267(1):126–132. [PubMed]
  • de Chastellier C, Thilo L. Phagosome maturation and fusion with lysosomes in relation to surface property and size of the phagocytic particle. Eur J Cell Biol. 1997 Sep;74(1):49–62. [PubMed]
  • Vieira OV, Botelho RJ, Rameh L, Brachmann SM, Matsuo T, Davidson HW, Schreiber A, Backer JM, Cantley LC, Grinstein S. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol. 2001 Oct 1;155(1):19–25. [PMC free article] [PubMed]
  • Fratti RA, Backer JM, Gruenberg J, Corvera S, Deretic V. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol. 2001 Aug 6;154(3):631–644. [PMC free article] [PubMed]
  • Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA, Deretic V. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem. 1997 May 16;272(20):13326–13331. [PubMed]
  • Clemens DL, Horwitz MA. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med. 1995 Jan 1;181(1):257–270. [PMC free article] [PubMed]
  • Desjardins M. Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 1995 May;5(5):183–186. [PubMed]
  • Wang YL, Goren MB. Differential and sequential delivery of fluorescent lysosomal probes into phagosomes in mouse peritoneal macrophages. J Cell Biol. 1987 Jun;104(6):1749–1754. [PMC free article] [PubMed]
  • Götte M, von Mollard GF. A new beat for the SNARE drum. Trends Cell Biol. 1998 Jun;8(6):215–218. [PubMed]
  • Chen YA, Scheller RH. SNARE-mediated membrane fusion. Nat Rev Mol Cell Biol. 2001 Feb;2(2):98–106. [PubMed]
  • Fasshauer D, Sutton RB, Brunger AT, Jahn R. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15781–15786. [PMC free article] [PubMed]
  • Rothman JE, Warren G. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol. 1994 Mar 1;4(3):220–233. [PubMed]
  • Pfeffer SR. Transport-vesicle targeting: tethers before SNAREs. Nat Cell Biol. 1999 May;1(1):E17–E22. [PubMed]
  • Söllner Thomas H. Vesicle tethers promoting fusion machinery assembly. Dev Cell. 2002 Apr;2(4):377–378. [PubMed]
  • Mullock BM, Smith CW, Ihrke G, Bright NA, Lindsay M, Parkinson EJ, Brooks DA, Parton RG, James DE, Luzio JP, et al. Syntaxin 7 is localized to late endosome compartments, associates with Vamp 8, and Is required for late endosome-lysosome fusion. Mol Biol Cell. 2000 Sep;11(9):3137–3153. [PMC free article] [PubMed]
  • Mullock BM, Bright NA, Fearon CW, Gray SR, Luzio JP. Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J Cell Biol. 1998 Feb 9;140(3):591–601. [PMC free article] [PubMed]
  • Pryor PR, Mullock BM, Bright NA, Gray SR, Luzio JP. The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol. 2000 May 29;149(5):1053–1062. [PMC free article] [PubMed]
  • Ward DM, Pevsner J, Scullion MA, Vaughn M, Kaplan J. Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol Biol Cell. 2000 Jul;11(7):2327–2333. [PMC free article] [PubMed]
  • Ward DM, Leslie JD, Kaplan J. Homotypic lysosome fusion in macrophages: analysis using an in vitro assay. J Cell Biol. 1997 Nov 3;139(3):665–673. [PMC free article] [PubMed]
  • Caplan S, Hartnell LM, Aguilar RC, Naslavsky N, Bonifacino JS. Human Vam6p promotes lysosome clustering and fusion in vivo. J Cell Biol. 2001 Jul 9;154(1):109–122. [PMC free article] [PubMed]
  • McBride HM, Rybin V, Murphy C, Giner A, Teasdale R, Zerial M. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell. 1999 Aug 6;98(3):377–386. [PubMed]
  • Antonin W, Holroyd C, Fasshauer D, Pabst S, Von Mollard GF, Jahn R. A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. EMBO J. 2000 Dec 1;19(23):6453–6464. [PMC free article] [PubMed]
  • Hackam DJ, Rotstein OD, Bennett MK, Klip A, Grinstein S, Manolson MF. Characterization and subcellular localization of target membrane soluble NSF attachment protein receptors (t-SNAREs) in macrophages. Syntaxins 2, 3, and 4 are present on phagosomal membranes. J Immunol. 1996 Jun 1;156(11):4377–4383. [PubMed]
  • Bajno L, Peng XR, Schreiber AD, Moore HP, Trimble WS, Grinstein S. Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation. J Cell Biol. 2000 May 1;149(3):697–706. [PMC free article] [PubMed]
  • Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M. The phagosome proteome: insight into phagosome functions. J Cell Biol. 2001 Jan 8;152(1):165–180. [PMC free article] [PubMed]
  • Funato K, Beron W, Yang CZ, Mukhopadhyay A, Stahl PD. Reconstitution of phagosome-lysosome fusion in streptolysin O-permeabilized cells. J Biol Chem. 1997 Jun 27;272(26):16147–16151. [PubMed]
  • Fasshauer D, Antonin W, Margittai M, Pabst S, Jahn R. Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties. J Biol Chem. 1999 May 28;274(22):15440–15446. [PubMed]
  • Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001 Feb;2(2):107–117. [PubMed]
  • Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B. Rab7: a key to lysosome biogenesis. Mol Biol Cell. 2000 Feb;11(2):467–480. [PMC free article] [PubMed]
  • McLauchlan H, Newell J, Morrice N, Osborne A, West M, Smythe E. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr Biol. 1998 Jan 1;8(1):34–45. [PubMed]
  • Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell. 1992 Sep 4;70(5):715–728. [PubMed]
  • Gorvel JP, Chavrier P, Zerial M, Gruenberg J. rab5 controls early endosome fusion in vitro. Cell. 1991 Mar 8;64(5):915–925. [PubMed]
  • Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M. Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol. 1999 Oct;1(6):376–382. [PubMed]
  • Roberts RL, Barbieri MA, Ullrich J, Stahl PD. Dynamics of rab5 activation in endocytosis and phagocytosis. J Leukoc Biol. 2000 Nov;68(5):627–632. [PubMed]
  • Stenmark H, Parton RG, Steele-Mortimer O, Lütcke A, Gruenberg J, Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 1994 Mar 15;13(6):1287–1296. [PMC free article] [PubMed]
  • Roberts RL, Barbieri MA, Pryse KM, Chua M, Morisaki JH, Stahl PD. Endosome fusion in living cells overexpressing GFP-rab5. J Cell Sci. 1999 Nov;112(Pt 21):3667–3675. [PubMed]
  • Barbieri MA, Roberts RL, Gumusboga A, Highfield H, Alvarez-Dominguez C, Wells A, Stahl PD. Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a. J Cell Biol. 2000 Oct 30;151(3):539–550. [PMC free article] [PubMed]
  • Li G, Barbieri MA, Colombo MI, Stahl PD. Structural features of the GTP-binding defective Rab5 mutants required for their inhibitory activity on endocytosis. J Biol Chem. 1994 May 20;269(20):14631–14635. [PubMed]
  • Li G, D'Souza-Schorey C, Barbieri MA, Cooper JA, Stahl PD. Uncoupling of membrane ruffling and pinocytosis during Ras signal transduction. J Biol Chem. 1997 Apr 18;272(16):10337–10340. [PubMed]
  • Barbieri MA, Kohn AD, Roth RA, Stahl PD. Protein kinase B/akt and rab5 mediate Ras activation of endocytosis. J Biol Chem. 1998 Jul 31;273(31):19367–19370. [PubMed]
  • Hoffenberg S, Liu X, Nikolova L, Hall HS, Dai W, Baughn RE, Dickey BF, Barbieri MA, Aballay A, Stahl PD, et al. A novel membrane-anchored Rab5 interacting protein required for homotypic endosome fusion. J Biol Chem. 2000 Aug 11;275(32):24661–24669. [PubMed]
  • Horiuchi H, Lippé R, McBride HM, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M, et al. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell. 1997 Sep 19;90(6):1149–1159. [PubMed]
  • Lippé R, Miaczynska M, Rybin V, Runge A, Zerial M. Functional synergy between Rab5 effector Rabaptin-5 and exchange factor Rabex-5 when physically associated in a complex. Mol Biol Cell. 2001 Jul;12(7):2219–2228. [PMC free article] [PubMed]
  • Mu FT, Callaghan JM, Steele-Mortimer O, Stenmark H, Parton RG, Campbell PL, McCluskey J, Yeo JP, Tock EP, Toh BH. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J Biol Chem. 1995 Jun 2;270(22):13503–13511. [PubMed]
  • Simonsen A, Lippé R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature. 1998 Jul 30;394(6692):494–498. [PubMed]
  • Callaghan J, Nixon S, Bucci C, Toh BH, Stenmark H. Direct interaction of EEA1 with Rab5b. Eur J Biochem. 1999 Oct 1;265(1):361–366. [PubMed]
  • Patki V, Virbasius J, Lane WS, Toh BH, Shpetner HS, Corvera S. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7326–7330. [PMC free article] [PubMed]
  • Gaullier JM, Simonsen A, D'Arrigo A, Bremnes B, Stenmark H, Aasland R. FYVE fingers bind PtdIns(3)P. Nature. 1998 Jul 30;394(6692):432–433. [PubMed]
  • Stenmark H, Aasland R, Toh BH, D'Arrigo A. Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J Biol Chem. 1996 Sep 27;271(39):24048–24054. [PubMed]
  • Liu K, Li G. Catalytic domain of the p120 Ras GAP binds to RAb5 and stimulates its GTPase activity. J Biol Chem. 1998 Apr 24;273(17):10087–10090. [PubMed]
  • Xiao GH, Shoarinejad F, Jin F, Golemis EA, Yeung RS. The tuberous sclerosis 2 gene product, tuberin, functions as a Rab5 GTPase activating protein (GAP) in modulating endocytosis. J Biol Chem. 1997 Mar 7;272(10):6097–6100. [PubMed]
  • Lanzetti L, Rybin V, Malabarba MG, Christoforidis S, Scita G, Zerial M, Di Fiore PP. The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature. 2000 Nov 16;408(6810):374–377. [PubMed]
  • Feng Y, Press B, Wandinger-Ness A. Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol. 1995 Dec;131(6 Pt 1):1435–1452. [PMC free article] [PubMed]
  • Vitelli R, Santillo M, Lattero D, Chiariello M, Bifulco M, Bruni CB, Bucci C. Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem. 1997 Feb 14;272(7):4391–4397. [PubMed]
  • Papini E, Satin B, Bucci C, de Bernard M, Telford JL, Manetti R, Rappuoli R, Zerial M, Montecucco C. The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J. 1997 Jan 2;16(1):15–24. [PMC free article] [PubMed]
  • Mukhopadhyay A, Funato K, Stahl PD. Rab7 regulates transport from early to late endocytic compartments in Xenopus oocytes. J Biol Chem. 1997 May 16;272(20):13055–13059. [PubMed]
  • Cantalupo G, Alifano P, Roberti V, Bruni CB, Bucci C. Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J. 2001 Feb 15;20(4):683–693. [PMC free article] [PubMed]
  • Alvarez-Dominguez C, Barbieri AM, Berón W, Wandinger-Ness A, Stahl PD. Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J Biol Chem. 1996 Jun 7;271(23):13834–13843. [PubMed]
  • Rupper A, Grove B, Cardelli J. Rab7 regulates phagosome maturation in Dictyostelium. J Cell Sci. 2001 Jul;114(Pt 13):2449–2460. [PubMed]
  • Toker A, Cantley LC. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature. 1997 Jun 12;387(6634):673–676. [PubMed]
  • Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001;70:535–602. [PubMed]
  • Backer JM. Phosphoinositide 3-kinases and the regulation of vesicular trafficking. Mol Cell Biol Res Commun. 2000 Apr;3(4):193–204. [PubMed]
  • Vanhaesebroeck B, Waterfield MD. Signaling by distinct classes of phosphoinositide 3-kinases. Exp Cell Res. 1999 Nov 25;253(1):239–254. [PubMed]
  • Volinia S, Dhand R, Vanhaesebroeck B, MacDougall LK, Stein R, Zvelebil MJ, Domin J, Panaretou C, Waterfield MD. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system. EMBO J. 1995 Jul 17;14(14):3339–3348. [PMC free article] [PubMed]
  • Panaretou C, Domin J, Cockcroft S, Waterfield MD. Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex. J Biol Chem. 1997 Jan 24;272(4):2477–2485. [PubMed]
  • Wurmser AE, Gary JD, Emr SD. Phosphoinositide 3-kinases and their FYVE domain-containing effectors as regulators of vacuolar/lysosomal membrane trafficking pathways. J Biol Chem. 1999 Apr 2;274(14):9129–9132. [PubMed]
  • Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip SC, Waterfield MD, Backer JM, Zerial M. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol. 1999 Aug;1(4):249–252. [PubMed]
  • Patki V, Lawe DC, Corvera S, Virbasius JV, Chawla A. A functional PtdIns(3)P-binding motif. Nature. 1998 Jul 30;394(6692):433–434. [PubMed]
  • Wishart MJ, Taylor GS, Dixon JE. Phoxy lipids: revealing PX domains as phosphoinositide binding modules. Cell. 2001 Jun 29;105(7):817–820. [PubMed]
  • Ellson Chris D, Andrews Simon, Stephens Len R, Hawkins Phill T. The PX domain: a new phosphoinositide-binding module. J Cell Sci. 2002 Mar 15;115(Pt 6):1099–1105. [PubMed]
  • Lawe DC, Patki V, Heller-Harrison R, Lambright D, Corvera S. The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization. J Biol Chem. 2000 Feb 4;275(5):3699–3705. [PubMed]
  • Li G, D'Souza-Schorey C, Barbieri MA, Roberts RL, Klippel A, Williams LT, Stahl PD. Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10207–10211. [PMC free article] [PubMed]
  • Jones AT, Mills IG, Scheidig AJ, Alexandrov K, Clague MJ. Inhibition of endosome fusion by wortmannin persists in the presence of activated Rab5. Mol Biol Cell. 1998 Feb;9(2):323–332. [PMC free article] [PubMed]
  • Nielsen E, Christoforidis S, Uttenweiler-Joseph S, Miaczynska M, Dewitte F, Wilm M, Hoflack B, Zerial M. Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol. 2000 Oct 30;151(3):601–612. [PMC free article] [PubMed]
  • Raiborg C, Bache KG, Mehlum A, Stang E, Stenmark H. Hrs recruits clathrin to early endosomes. EMBO J. 2001 Sep 3;20(17):5008–5021. [PMC free article] [PubMed]
  • Raiborg Camilla, Bache Kristi G, Gillooly David J, Madshus Inger Helene, Stang Espen, Stenmark Harald. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol. 2002 May;4(5):394–398. [PubMed]
  • Sachse Martin, Urbé Sylvie, Oorschot Viola, Strous Ger J, Klumperman Judith. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell. 2002 Apr;13(4):1313–1328. [PMC free article] [PubMed]
  • Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 2000 Sep 1;19(17):4577–4588. [PMC free article] [PubMed]
  • Shisheva A, Sbrissa D, Ikonomov O. Cloning, characterization, and expression of a novel Zn2+-binding FYVE finger-containing phosphoinositide kinase in insulin-sensitive cells. Mol Cell Biol. 1999 Jan;19(1):623–634. [PMC free article] [PubMed]
  • Sbrissa D, Ikonomov OC, Shisheva A. PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin. J Biol Chem. 1999 Jul 30;274(31):21589–21597. [PubMed]
  • Odorizzi G, Babst M, Emr SD. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell. 1998 Dec 11;95(6):847–858. [PubMed]
  • Gary JD, Wurmser AE, Bonangelino CJ, Weisman LS, Emr SD. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol. 1998 Oct 5;143(1):65–79. [PMC free article] [PubMed]
  • Ikonomov OC, Sbrissa D, Shisheva A. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J Biol Chem. 2001 Jul 13;276(28):26141–26147. [PubMed]
  • Araki N, Johnson MT, Swanson JA. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol. 1996 Dec;135(5):1249–1260. [PMC free article] [PubMed]
  • Crowley MT, Costello PS, Fitzer-Attas CJ, Turner M, Meng F, Lowell C, Tybulewicz VL, DeFranco AL. A critical role for Syk in signal transduction and phagocytosis mediated by Fcgamma receptors on macrophages. J Exp Med. 1997 Oct 6;186(7):1027–1039. [PMC free article] [PubMed]
  • Cox D, Tseng CC, Bjekic G, Greenberg S. A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J Biol Chem. 1999 Jan 15;274(3):1240–1247. [PubMed]
  • Marshall JG, Booth JW, Stambolic V, Mak T, Balla T, Schreiber AD, Meyer T, Grinstein S. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis. J Cell Biol. 2001 Jun 25;153(7):1369–1380. [PMC free article] [PubMed]
  • Kanai F, Liu H, Field SJ, Akbary H, Matsuo T, Brown GE, Cantley LC, Yaffe MB. The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat Cell Biol. 2001 Jul;3(7):675–678. [PubMed]
  • Haurani FI, Ryter A. Tracing iron and transferrin in the macrophage by visual means. Am J Hematol. 1993 Nov;44(3):179–186. [PubMed]
  • Ryter A. Relationship between ultrastructure and specific functions of macrophages. Comp Immunol Microbiol Infect Dis. 1985;8(2):119–133. [PubMed]
  • Muller WA, Steinman RM, Cohn ZA. Membrane proteins of the vacuolar system. III. Further studies on the composition and recycling of endocytic vacuole membrane in cultured macrophages. J Cell Biol. 1983 Jan;96(1):29–36. [PMC free article] [PubMed]
  • Stoorvogel W, Oorschot V, Geuze HJ. A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol. 1996 Jan;132(1-2):21–33. [PMC free article] [PubMed]
  • Aniento F, Gu F, Parton RG, Gruenberg J. An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol. 1996 Apr;133(1):29–41. [PMC free article] [PubMed]
  • Cosson P, Letourneur F. Coatomer (COPI)-coated vesicles: role in intracellular transport and protein sorting. Curr Opin Cell Biol. 1997 Aug;9(4):484–487. [PubMed]
  • Schekman R, Orci L. Coat proteins and vesicle budding. Science. 1996 Mar 15;271(5255):1526–1533. [PubMed]
  • Lippincott-Schwartz J, Yuan L, Tipper C, Amherdt M, Orci L, Klausner RD. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell. 1991 Nov 1;67(3):601–616. [PubMed]
  • Gu F, Aniento F, Parton RG, Gruenberg J. Functional dissection of COP-I subunits in the biogenesis of multivesicular endosomes. J Cell Biol. 1997 Dec 1;139(5):1183–1195. [PMC free article] [PubMed]
  • Daro E, Sheff D, Gomez M, Kreis T, Mellman I. Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J Cell Biol. 1997 Dec 29;139(7):1747–1759. [PMC free article] [PubMed]
  • Palmer DJ, Helms JB, Beckers CJ, Orci L, Rothman JE. Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J Biol Chem. 1993 Jun 5;268(16):12083–12089. [PubMed]
  • Helms JB, Rothman JE. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature. 1992 Nov 26;360(6402):352–354. [PubMed]
  • Donaldson JG, Cassel D, Kahn RA, Klausner RD. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein beta-COP to Golgi membranes. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6408–6412. [PMC free article] [PubMed]
  • Guo Q, Vasile E, Krieger M. Disruptions in Golgi structure and membrane traffic in a conditional lethal mammalian cell mutant are corrected by epsilon-COP. J Cell Biol. 1994 Jun;125(6):1213–1224. [PMC free article] [PubMed]
  • Hobbie L, Fisher AS, Lee S, Flint A, Krieger M. Isolation of three classes of conditional lethal Chinese hamster ovary cell mutants with temperature-dependent defects in low density lipoprotein receptor stability and intracellular membrane transport. J Biol Chem. 1994 Aug 19;269(33):20958–20970. [PubMed]
  • Berón W, Mayorga LS, Colombo MI, Stahl PD. Recruitment of coat-protein-complex proteins on to phagosomal membranes is regulated by a brefeldin A-sensitive ADP-ribosylation factor. Biochem J. 2001 Apr 15;355(Pt 2):409–415. [PMC free article] [PubMed]
  • Prekeris R, Klumperman J, Chen YA, Scheller RH. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J Cell Biol. 1998 Nov 16;143(4):957–971. [PMC free article] [PubMed]
  • Newmyer SL, Schmid SL. Dominant-interfering Hsc70 mutants disrupt multiple stages of the clathrin-coated vesicle cycle in vivo. J Cell Biol. 2001 Feb 5;152(3):607–620. [PMC free article] [PubMed]
  • Nicoziani P, Vilhardt F, Llorente A, Hilout L, Courtoy PJ, Sandvig K, van Deurs B. Role for dynamin in late endosome dynamics and trafficking of the cation-independent mannose 6-phosphate receptor. Mol Biol Cell. 2000 Feb;11(2):481–495. [PMC free article] [PubMed]
  • Pierre P, Scheel J, Rickard JE, Kreis TE. CLIP-170 links endocytic vesicles to microtubules. Cell. 1992 Sep 18;70(6):887–900. [PubMed]
  • Sheetz MP. Microtubule motor complexes moving membranous organelles. Cell Struct Funct. 1996 Oct;21(5):369–373. [PubMed]
  • Drewes G, Ebneth A, Mandelkow EM. MAPs, MARKs and microtubule dynamics. Trends Biochem Sci. 1998 Aug;23(8):307–311. [PubMed]
  • Hunter AW, Wordeman L. How motor proteins influence microtubule polymerization dynamics. J Cell Sci. 2000 Dec;113(Pt 24):4379–4389. [PubMed]
  • Maccioni RB, Cambiazo V. Role of microtubule-associated proteins in the control of microtubule assembly. Physiol Rev. 1995 Oct;75(4):835–864. [PubMed]
  • Matteoni R, Kreis TE. Translocation and clustering of endosomes and lysosomes depends on microtubules. J Cell Biol. 1987 Sep;105(3):1253–1265. [PMC free article] [PubMed]
  • Gruenberg J, Griffiths G, Howell KE. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol. 1989 Apr;108(4):1301–1316. [PMC free article] [PubMed]
  • Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol. 1997 Oct 20;139(2):469–484. [PMC free article] [PubMed]
  • Aniento F, Emans N, Griffiths G, Gruenberg J. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J Cell Biol. 1993 Dec;123(6 Pt 1):1373–1387. [PMC free article] [PubMed]
  • Toyohara A, Inaba K. Transport of phagosomes in mouse peritoneal macrophages. J Cell Sci. 1989 Sep;94(Pt 1):143–153. [PubMed]
  • Blocker A, Severin FF, Burkhardt JK, Bingham JB, Yu H, Olivo JC, Schroer TA, Hyman AA, Griffiths G. Molecular requirements for bi-directional movement of phagosomes along microtubules. J Cell Biol. 1997 Apr 7;137(1):113–129. [PMC free article] [PubMed]
  • Blocker A, Griffiths G, Olivo JC, Hyman AA, Severin FF. A role for microtubule dynamics in phagosome movement. J Cell Sci. 1998 Feb;111(Pt 3):303–312. [PubMed]
  • Pesanti EL, Axline SG. Phagolysosome formation in normal and colchicine-treated macrophages. J Exp Med. 1975 Oct 1;142(4):903–913. [PMC free article] [PubMed]
  • Blocker A, Severin FF, Habermann A, Hyman AA, Griffiths G, Burkhardt JK. Microtubule-associated protein-dependent binding of phagosomes to microtubules. J Biol Chem. 1996 Feb 16;271(7):3803–3811. [PubMed]
  • Bielli A, Thörnqvist PO, Hendrick AG, Finn R, Fitzgerald K, McCaffrey MW. The small GTPase Rab4A interacts with the central region of cytoplasmic dynein light intermediate chain-1. Biochem Biophys Res Commun. 2001 Mar;281(5):1141–1153. [PubMed]
  • Mammoto A, Ohtsuka T, Hotta I, Sasaki T, Takai Y. Rab11BP/Rabphilin-11, a downstream target of rab11 small G protein implicated in vesicle recycling. J Biol Chem. 1999 Sep 3;274(36):25517–25524. [PubMed]
  • Gavin RH. Microtubule-microfilament synergy in the cytoskeleton. Int Rev Cytol. 1997;173:207–242. [PubMed]
  • Kelleher JF, Titus MA. Intracellular motility: how can we all work together? Curr Biol. 1998 May 21;8(11):R394–R397. [PubMed]
  • DePina AS, Langford GM. Vesicle transport: the role of actin filaments and myosin motors. Microsc Res Tech. 1999 Oct 15;47(2):93–106. [PubMed]
  • Taunton J, Rowning BA, Coughlin ML, Wu M, Moon RT, Mitchison TJ, Larabell CA. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol. 2000 Feb 7;148(3):519–530. [PMC free article] [PubMed]
  • Taunton J. Actin filament nucleation by endosomes, lysosomes and secretory vesicles. Curr Opin Cell Biol. 2001 Feb;13(1):85–91. [PubMed]
  • van Deurs B, Holm PK, Kayser L, Sandvig K. Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. Eur J Cell Biol. 1995 Apr;66(4):309–323. [PubMed]
  • Raposo G, Cordonnier MN, Tenza D, Menichi B, Dürrbach A, Louvard D, Coudrier E. Association of myosin I alpha with endosomes and lysosomes in mammalian cells. Mol Biol Cell. 1999 May;10(5):1477–1494. [PMC free article] [PubMed]
  • Desjardins M, Celis JE, van Meer G, Dieplinger H, Jahraus A, Griffiths G, Huber LA. Molecular characterization of phagosomes. J Biol Chem. 1994 Dec 23;269(51):32194–32200. [PubMed]
  • Defacque H, Egeberg M, Habermann A, Diakonova M, Roy C, Mangeat P, Voelter W, Marriott G, Pfannstiel J, Faulstich H, et al. Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO J. 2000 Jan 17;19(2):199–212. [PMC free article] [PubMed]
  • Morrissette NS, Gold ES, Guo J, Hamerman JA, Ozinsky A, Bedian V, Aderem AA. Isolation and characterization of monoclonal antibodies directed against novel components of macrophage phagosomes. J Cell Sci. 1999 Dec;112(Pt 24):4705–4713. [PubMed]
  • Möller W, Nemoto I, Matsuzaki T, Hofer T, Heyder J. Magnetic phagosome motion in J774A.1 macrophages: influence of cytoskeletal drugs. Biophys J. 2000 Aug;79(2):720–730. [PMC free article] [PubMed]
  • Jahraus A, Egeberg M, Hinner B, Habermann A, Sackman E, Pralle A, Faulstich H, Rybin V, Defacque H, Griffiths G. ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol Biol Cell. 2001 Jan;12(1):155–170. [PMC free article] [PubMed]
  • Tilney LG, Connelly PS, Portnoy DA. Actin filament nucleation by the bacterial pathogen, Listeria monocytogenes. J Cell Biol. 1990 Dec;111(6 Pt 2):2979–2988. [PMC free article] [PubMed]
  • Defacque H, Egeberg M, Antzberger A, Ansorge W, Way M, Griffiths G. Actin assembly induced by polylysine beads or purified phagosomes: quantitation by a new flow cytometry assay. Cytometry. 2000 Sep 1;41(1):46–54. [PubMed]
  • Tsukita S, Oishi K, Sato N, Sagara J, Kawai A, Tsukita S. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol. 1994 Jul;126(2):391–401. [PMC free article] [PubMed]
  • Holm A, Tejle K, Magnusson KE, Descoteaux A, Rasmusson B. Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: correlation with impaired translocation of PKCalpha and defective phagosome maturation. Cell Microbiol. 2001 Jul;3(7):439–447. [PubMed]
  • Vergne I, Constant P, Lanéelle G. Phagosomal pH determination by dual fluorescence flow cytometry. Anal Biochem. 1998 Jan 1;255(1):127–132. [PubMed]
  • Lukacs GL, Rotstein OD, Grinstein S. Phagosomal acidification is mediated by a vacuolar-type H(+)-ATPase in murine macrophages. J Biol Chem. 1990 Dec 5;265(34):21099–21107. [PubMed]
  • Tapper H, Sundler R. Bafilomycin A1 inhibits lysosomal, phagosomal, and plasma membrane H(+)-ATPase and induces lysosomal enzyme secretion in macrophages. J Cell Physiol. 1995 Apr;163(1):137–144. [PubMed]
  • van Deurs B, Holm PK, Sandvig K. Inhibition of the vacuolar H(+)-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in HEp-2 cells. Eur J Cell Biol. 1996 Apr;69(4):343–350. [PubMed]
  • Bayer N, Schober D, Prchla E, Murphy RF, Blaas D, Fuchs R. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J Virol. 1998 Dec;72(12):9645–9655. [PMC free article] [PubMed]
  • van Weert AW, Dunn KW, Geuze HJ, Maxfield FR, Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol. 1995 Aug;130(4):821–834. [PMC free article] [PubMed]
  • D'Arrigo A, Bucci C, Toh BH, Stenmark H. Microtubules are involved in bafilomycin A1-induced tubulation and Rab5-dependent vacuolation of early endosomes. Eur J Cell Biol. 1997 Feb;72(2):95–103. [PubMed]
  • Maranda B, Brown D, Bourgoin S, Casanova JE, Vinay P, Ausiello DA, Marshansky V. Intra-endosomal pH-sensitive recruitment of the Arf-nucleotide exchange factor ARNO and Arf6 from cytoplasm to proximal tubule endosomes. J Biol Chem. 2001 May 25;276(21):18540–18550. [PubMed]
  • Gu F, Gruenberg J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J Biol Chem. 2000 Mar 17;275(11):8154–8160. [PubMed]
  • Russell DG. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol. 2001 Aug;2(8):569–577. [PubMed]
  • McNeil PL, Tanasugarn L, Meigs JB, Taylor DL. Acidification of phagosomes is initiated before lysosomal enzyme activity is detected. J Cell Biol. 1983 Sep;97(3):692–702. [PMC free article] [PubMed]
  • Hart PD, Young MR. Ammonium chloride, an inhibitor of phagosome-lysosome fusion in macrophages, concurrently induces phagosome-endosome fusion, and opens a novel pathway: studies of a pathogenic mycobacterium and a nonpathogenic yeast. J Exp Med. 1991 Oct 1;174(4):881–889. [PMC free article] [PubMed]
  • Gordon AH, Hart PD, Young MR. Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature. 1980 Jul 3;286(5768):79–80. [PubMed]
  • Kielian MC, Steinman RM, Cohn ZA. Intralysosomal accumulation of polyanions. I. Fusion of pinocytic and phagocytic vacuoles with secondary lysosomes. J Cell Biol. 1982 Jun;93(3):866–874. [PMC free article] [PubMed]
  • Brumell JH, Volchuk A, Sengelov H, Borregaard N, Cieutat AM, Bainton DF, Grinstein S, Klip A. Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments. J Immunol. 1995 Dec 15;155(12):5750–5759. [PubMed]
  • Kim-Park WK, Moore MA, Hakki ZW, Kowolik MJ. Activation of the neutrophil respiratory burst requires both intracellular and extracellular calcium. Ann N Y Acad Sci. 1997 Dec 15;832:394–404. [PubMed]
  • Mandeville JT, Maxfield FR. Calcium and signal transduction in granulocytes. Curr Opin Hematol. 1996 Jan;3(1):63–70. [PubMed]
  • Stendahl O, Krause KH, Krischer J, Jerström P, Theler JM, Clark RA, Carpentier JL, Lew DP. Redistribution of intracellular Ca2+ stores during phagocytosis in human neutrophils. Science. 1994 Sep 2;265(5177):1439–1441. [PubMed]
  • Malik ZA, Denning GM, Kusner DJ. Inhibition of Ca(2+) signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J Exp Med. 2000 Jan 17;191(2):287–302. [PMC free article] [PubMed]
  • Mills IG, Urbé S, Clague MJ. Relationships between EEA1 binding partners and their role in endosome fusion. J Cell Sci. 2001 May;114(Pt 10):1959–1965. [PubMed]
  • Holroyd C, Kistner U, Annaert W, Jahn R. Fusion of endosomes involved in synaptic vesicle recycling. Mol Biol Cell. 1999 Sep;10(9):3035–3044. [PMC free article] [PubMed]
  • Peters C, Mayer A. Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature. 1998 Dec 10;396(6711):575–580. [PubMed]
  • Lundqvist-Gustafsson H, Gustafsson M, Dahlgren C. Dynamic ca(2+)changes in neutrophil phagosomes A source for intracellular ca(2+)during phagolysosome formation? Cell Calcium. 2000 Jun;27(6):353–362. [PubMed]
  • Colombo MI, Beron W, Stahl PD. Calmodulin regulates endosome fusion. J Biol Chem. 1997 Mar 21;272(12):7707–7712. [PubMed]
  • Wickner W, Haas A. Yeast homotypic vacuole fusion: a window on organelle trafficking mechanisms. Annu Rev Biochem. 2000;69:247–275. [PubMed]
  • Zimmerli S, Majeed M, Gustavsson M, Stendahl O, Sanan DA, Ernst JD. Phagosome-lysosome fusion is a calcium-independent event in macrophages. J Cell Biol. 1996 Jan;132(1-2):49–61. [PMC free article] [PubMed]
  • Jaconi ME, Lew DP, Carpentier JL, Magnusson KE, Sjögren M, Stendahl O. Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. J Cell Biol. 1990 May;110(5):1555–1564. [PMC free article] [PubMed]
  • Downey GP, Botelho RJ, Butler JR, Moltyaner Y, Chien P, Schreiber AD, Grinstein S. Phagosomal maturation, acidification, and inhibition of bacterial growth in nonphagocytic cells transfected with FcgammaRIIA receptors. J Biol Chem. 1999 Oct 1;274(40):28436–28444. [PubMed]
  • Wilsson A, Lundqvist H, Gustafsson M, Stendahl O. Killing of phagocytosed Staphylococcus aureus by human neutrophils requires intracellular free calcium. J Leukoc Biol. 1996 Jun;59(6):902–907. [PubMed]
  • Bengtsson T, Jaconi ME, Gustafson M, Magnusson KE, Theler JM, Lew DP, Stendahl O. Actin dynamics in human neutrophils during adhesion and phagocytosis is controlled by changes in intracellular free calcium. Eur J Cell Biol. 1993 Oct;62(1):49–58. [PubMed]
  • Ferrari G, Langen H, Naito M, Pieters J. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell. 1999 May 14;97(4):435–447. [PubMed]
  • Greenberg S, el Khoury J, di Virgilio F, Kaplan EM, Silverstein SC. Ca(2+)-independent F-actin assembly and disassembly during Fc receptor-mediated phagocytosis in mouse macrophages. J Cell Biol. 1991 May;113(4):757–767. [PMC free article] [PubMed]
  • Ernst JD. Annexin III translocates to the periphagosomal region when neutrophils ingest opsonized yeast. J Immunol. 1991 May 1;146(9):3110–3114. [PubMed]
  • Majeed M, Perskvist N, Ernst JD, Orselius K, Stendahl O. Roles of calcium and annexins in phagocytosis and elimination of an attenuated strain of Mycobacterium tuberculosis in human neutrophils. Microb Pathog. 1998 May;24(5):309–320. [PubMed]
  • Malik ZA, Iyer SS, Kusner DJ. Mycobacterium tuberculosis phagosomes exhibit altered calmodulin-dependent signal transduction: contribution to inhibition of phagosome-lysosome fusion and intracellular survival in human macrophages. J Immunol. 2001 Mar 1;166(5):3392–3401. [PubMed]
  • Yi J, Tang XM. The convergent point of the endocytic and autophagic pathways in leydig cells. Cell Res. 1999 Dec;9(4):243–253. [PubMed]
  • Yokota S. Formation of autophagosomes during degradation of excess peroxisomes induced by administration of dioctyl phthalate. Eur J Cell Biol. 1993 Jun;61(1):67–80. [PubMed]
  • Ueno T, Muno D, Kominami E. Membrane markers of endoplasmic reticulum preserved in autophagic vacuolar membranes isolated from leupeptin-administered rat liver. J Biol Chem. 1991 Oct 5;266(28):18995–18999. [PubMed]
  • Lord JM, Davey J, Frigerio L, Roberts LM. Endoplasmic reticulum-associated protein degradation. Semin Cell Dev Biol. 2000 Jun;11(3):159–164. [PubMed]
  • Ishiguro T, Nakajima M, Naito M, Muto T, Tsuruo T. Identification of genes differentially expressed in B16 murine melanoma sublines with different metastatic potentials. Cancer Res. 1996 Feb 15;56(4):875–879. [PubMed]
  • Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y. A protein conjugation system essential for autophagy. Nature. 1998 Sep 24;395(6700):395–398. [PubMed]
  • Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol. 2001 Feb 19;152(4):657–668. [PMC free article] [PubMed]
  • Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001 Mar;2(3):211–216. [PubMed]

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